On the Origin and Evolution of True Crabs: Insights from Tropical America by Javier Luque A thesis submitted in partial fulfillment of the requirements for the degree of Doctor of Philosophy in SYSTEMATICS AND EVOLUTION Department of Biological Sciences University of Alberta © Javier Luque, 2018 Abstract A full understanding of the evolution of novel forms requires inference about their origins through the study of variation in extant taxa and clues from the fossil record. However, the origins of morphological diversity in many groups are obscured by the scarcity of transitional fossils or reliable early occurrences of crown groups near the base of major branches. This is the case for true crabs, or Brachyura, a group whose evolutionary history and internal phylogenetic relationships remain unresolved. Although molecular and morphological phylogenetics bring powerful tools to the study of relatedness at the genotypic and phenotypic levels, the fossil record provides a unique glimpse into the origins of such relatedness by revealing a past morphological diversity otherwise inaccessible. Furthermore, fossils are pivotal for understanding the evolution of key traits, and provide geographic and chronologic data critical to the calibration of nodes of interest. Unfortunately, in spite of the overall good crab fossil record in Late Cretaceous and Cenozoic deposits worldwide, records of early brachyurans are still poorly known, and a strong collection bias towards modern high latitudes limits our understanding of the origins of the group’s origin and early morphological variation. Here I examine the fossil record of true crabs from the tropical Americas based on newly discovered crustacean-rich assemblages from the Early and ‘mid’ Cretaceous and re- examination of museum specimens, with emphasis on some brachyuran higher taxa (e.g., Raninoida, Eubrachyura, and a new chimaeric lineage described herein). I test hypotheses about the relationships among the main fossil brachyuran lineages, and investigate the distribution of visual systems in ‘intermediate’ brachyuran groups. Analyses of morphological data from fossil and extant taxa support the view that podotreme brachyurans (crabs with sexual openings at the base of the legs) form a paraphyletic grade, and that some derived podotreme groups might be ii closer to Eubrachyura or ‘higher’ true crabs than to less inclusive podotremes. New Cretaceous fossils push the envelope for what a ‘crab’ is, and challenge conventional views of crab evolution. My findings show that the evolution of shovel-like and paddle-like pereiopods, and decarcinization, or loss of a typical ‘crab-like’ form, have occurred independently at least five times since the Early Cretaceous or before. Similarly, my findings reveal that the loss of the plesiomorphic ‘mirror’ eyes — seen among most decapod crustaceans including the earliest brachyurans — has occurred in several podotremes and in eubrachyurans since at least the Early Cretaceous. In addition, the distribution of eye types among brachyuran crabs supports a paraphyletic podotreme grade, as suggested by recent phylogenetic works. The versatility of the crab body form, and the interplay between development and ecological invasion, may have acted as drivers of morphological innovation. These findings provide novel insights about the time, place, and phylogenetic pathways of early diversification in crabs, with the aim of contributing to the vast ongoing inter–institutional effort to resolve the Decapoda Tree of Life. iii Preface Chapter 2 has been published as Luque, J. (2015) The oldest higher true crabs (Crustacea: Decapoda: Eubrachyura): insights from the Early Cretaceous of the Americas. Palaeontology 58(2): 251–263. http://onlinelibrary.wiley.com/doi/10.1111/pala.12135/full. Chapter 3 has been published as Luque, J. (2015) A puzzling frog crab (Crustacea: Decapoda: Brachyura) from the Early Cretaceous Santana Group of Brazil: frog first or crab first? Journal of Systematic Palaeontology 13(2): 153–166 http://dx.doi.org/10.1080/14772019.2013.871586. Chapter 4 is near submission as Luque, J., Feldmann, R.M., Vernygora, O., Schweitzer, C.E., Cameron, C.B., Kerr, K.A., Vega, F.J., Duque, A., Strange, M., Palmer, A.R., & Jaramillo, C. Exceptional preservation of a chimaera crab from the Cretaceous unveils the evolution of a novel body form. J.L. conceived and designed the study, discovered the Colombian material, prepared the specimens, studied and described the material. M.S. discovered the US material. J.L., R.M.F, C.E.S. constructed the dataset. J.L., O.V., C.B.C. analyzed the data. A.D. designed the digital reconstructions and 3D animations. R.M.F., C.E.S., K.A.K., C.B.C., A.R.P., C.J. contributed logistics/materials/analysis tools. J.L. wrote the paper and made the line drawings, figures, and tables. O.V. made the Supplementary Figures S4.8 and S4.9. J.L., K.A.K., R.M.F., C.E.S., O.V., F.J.V., C.B.C., A.R.P., C.J. edited the manuscript. Chapter 5 has been published as Luque, J., Schweitzer, C.E., Santana, W., Portell, R.W., Vega, F.J., and Klompmaker, A.A. (2017) Checklist of fossil decapod crustaceans from tropical America, Part I: Anomura and Brachyura. Nauplius 25: e2017025 https://doi.org/10.1590/2358-2936e2017025. JL conceived and designed the study, analyzed the data, wrote the paper, and made Figures 5.1–5.4, 5.6–5.10, and Chart 5.17. WS made a draft of Figure 5.5; RWP a draft of Figures 5.11, 5.12, 5.14– 5.16; and FJV a drat of Figure 5.13. JL edited and All authors contributed data and edited the manuscript. Chapter 6 is a work in progress, and aims to be a mixed review and data paper about the distribution of visual systems in fossil and extant true crabs. iv Dedication In memory of my father, who always encouraged me to follow my dream of becoming an ‘- ologist’ (geologist, biologist, palaeontologist). To my mother, who together with my father, instilled in me a deep passion and appreciation for nature, and for never getting mad at me for bringing home every possible rock and dead critter I found in our camping trips in the Andes. Their constant support and encouragement paved the road I walk today. To Livia, my best furry friend, who I dearly miss every day, and to Sailor and Mona (a.k.a. Sweet Pea), for bringing so much joy to our lives (pure entertainment). And especially to Kecia, the sun of my life, whose shining light illuminates my steps. To them, my eternal gratitude, my eternal love. v Acknowledgements This work was possible thanks to the generosity of several sources that provided partial funding during the tenure of my PhD, in particular the Natural Science and Engineering Research Council of Canada (NSERC) Canada Graduate Scholarship (CGS–D), the Izaak Walton Killam Memorial Scholarship, the Andrew Stewart Memorial Graduate Prize, the University of Alberta President’s Doctoral Prize of Distinction, the Devendra Jindal Graduate Scholarship, the Alberta Society of Professional Biologists Graduate Scholarship, and the Kay Ball Memorial Graduate Student Research Travel Award (Canada). Additional support was provided by the NSERC Discovery Grant A7245 and RGPIN 04863 to A. Rich Palmer. Thanks also to the Smithsonian Tropical Research Institute Short (Panama), the Fondo Corrigan-ACGGP-ARES (Colombia), the Sedimentary Geology, Time, Environment, Paleontology, Paleoclimatology & Energy (STEPPE) and the National Science Foundation (NSF) Student Travel Award Grant (USA). Special thanks to Carlos Jaramillo, one of my mentors, and who has supported much of my research and fieldwork during my career. To Chris Cameron, also a mentor and friend, thanks to whom I ended up coming to the University of Alberta for my Ph.D. To John Christy, Rodney Feldmann and Carrie Schweitzer, Francisco Vega, Barry van Bakel, Àlex Ossó, Danièle Guinot, Roger Portell, Austing Hendy, Adiël Klompmaker, William Santana, Thomas Hegna, and Jo Wolfe for their friendship and intellectual support. Thanks to Prof. Fernando Etayo- Serna, to Roberto Terraza, and Diana Montoya, for field support and information regarding the stratigraphic position of the material studied in Chapter 2. To Alessandro Garassino, Hiroaki Karasawa, and John E. Simes, for providing images of type specimens illustrated in Chapter 2. To Paula Sucerquia, Rodney Feldmann, Barry Van Bakel, and Roger Portell, for thoughtful discussions and providing photos of specimens illustrated in Chapter 3. To John Maisey, Lorraine Meeker and Chester Tarka, for the photos of the Cretaceous brachyuran larva illustrated in Chapter 3. To Christopher Boyko, Arthur Anker, Tin Yam Chan, and Hans Hillewaert for some of the images of extant crabs illustrated in Chapter 4. To Sylvain Charbonnier, Jocelyn Falconnet, Peter Massicard, Rodney Feldmann, Roger Portell, Sean Rogers, Francisco Vega, and William Santana, for providing images of fossil specimens illustrated in Chapter 5. vi To Gale Bishop, Bruce Thiel, Àlex Ossó, and Rick Ross, for their enormous generosity providing literature and reference materials. To Jose Arenas, Mauricio Pardo, and the Colombian Geological Survey, for providing export permits and field support. To Rafael Lemaitre, Karen Reed, and Daniel Levin, for help accessing the United States National Museum of Natural History (Smithsonian Institution) Zoology and Palaeobiology collections. To Peter Davie, for help accessing the QMW Invertebrate Zoology collections at the Queensland Museum, Brisbane, Australia. To Roger Portell for help accessing the Invertebrate Paleontology collections at the Florida Museum of Natural History, University of Florida, Gainesville, Florida. To Sylvain Charbonnier, Paula Martin-Lefebre, and Laure Corbaire, for help accessing the Palaeontology and Invertebrate Zoology collections at the Muséum national d’Histoire naturelle, Paris, France. To the Autoridad del Canal de Panamá (ACP) for providing laboratory facilities; the Dirección de Recursos Minerales de Panamá for facilitating collecting and export permits; Ricardo Perez for donating the Toyota vehicles used for fieldwork in Panama. To Arelene Oatway, Nathan Gerein, and Jorge Ceballos, for microscopy lab assistance.